EGFR and Notch signaling respectively regulate proliferative activity and multiple cell lineage differentiation of Drosophila gastric stem cells

Cell Research

Volumn 24, Issue 5, 2014, Pages 610-627

  Wang, Chenhui ^a,b   Guo, Xingting ^a,b   Xi, Rongwen ^a  

^a NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

^b BEIJING NORMAL UNIVERSITY   (China)

Author keywords

copper cell; Drosophila; EGFR; gastric stem cell (GSSC); interstitial cell; lineage differentiation; Notch

Indexed keywords

DROSOPHILA PROTEIN; EGFR PROTEIN, DROSOPHILA; EPIDERMAL GROWTH FACTOR RECEPTOR; NOTCH PROTEIN, DROSOPHILA; NOTCH RECEPTOR; RECEPTOR; WG PROTEIN, DROSOPHILA; WNT1 PROTEIN;

ANIMAL; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CYTOLOGY; DROSOPHILA; ENTEROENDOCRINE CELL; METABOLISM; MULTIPOTENT STEM CELL; SIGNAL TRANSDUCTION; STOMACH MUCOSA;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; DROSOPHILA; DROSOPHILA PROTEINS; ENTEROENDOCRINE CELLS; GASTRIC MUCOSA; MULTIPOTENT STEM CELLS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, INVERTEBRATE PEPTIDE; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; WNT1 PROTEIN;

EID: 84899934624     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2014.27     Document Type: Article

References (56)

1. Schepers A, Clevers H. Wnt signaling, stem cells, and cancer of the gastrointestinal tract. Cold Spring Harb Perspect Biol 2012; 4:a007989.
2. Dubreuil RR. Copper cells and stomach acid secretion in the Drosophila midgut. Int J Biochem Cell Biol 2004; 36:745-752.
3. Strand M, Micchelli CA. Quiescent gastric stem cells maintain the adult Drosophila stomach. Proc Natl Acad Sci USA 2011; 108:17696-17701.
4. Takashima S, Hartenstein V. Genetic control of intestinal stem cell specifcation and development: a comparative view. Stem Cell Rev 2012; 8:597-608.
5. Ohlstein B, Spradling A. The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 2006; 439:470-474.
6. Micchelli CA, Perrimon N. Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 2006; 439:475-479.
7. Ohlstein B, Spradling A. Multipotent Drosophila intestinal stem cells specify daughter cell fates by differential notch signaling. Science 2007; 315:988-992.
8. Jiang H, Grenley MO, Bravo MJ, Blumhagen RZ, Edgar BA. EGFR/Ras/MAPK signaling mediates adult midgut epithelial homeostasis and regeneration in Drosophila. Cell Stem Cell 2011; 8:84-95.
9. Xu N, Wang SQ, Tan D, Gao Y, Lin G, Xi R. EGFR, Wingless and JAK/STAT signaling cooperatively maintain Drosophila intestinal stem cells. Dev Biol 2011; 354:31-43.
10. Biteau B, Jasper H. EGF signaling regulates the proliferation of intestinal stem cells in Drosophila. Development 2011; 138:1045-1055.
11. Buchon N, Broderick NA, Kuraishi T, Lemaitre B. Drosophila EGFR pathway coordinates stem cell proliferation and gut remodeling following infection. BMC Biol 2010; 8:152.
12. Jiang H, Patel PH, Kohlmaier A, Grenley MO, McEwen DG, Edgar BA. Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 2009; 137:1343-1355.
13. Sandu C, Ryoo HD, Steller H. Drosophila IAP antagonists form multimeric complexes to promote cell death. J Cell Biol 2010; 190:1039-1052.
14. Lin G, Zhang X, Ren J, et al. Integrin signaling is required for maintenance and proliferation of intestinal stem cells in Dro-sophila. Dev Biol 2013; 377:177-187.
15. Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993; 11 8:401-415.
16. McGuire SE, Mao Z, Davis RL. Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila. Sci STKE 2004; 2004:pl6.
17. Hay BA, Wolff T, Rubin GM. Expression of baculovirus P35 prevents cell death in Drosophila. Development 1994; 120:2121-2129.
18. Clem RJ, Fechheimer M, Miller LK. Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science 1991; 254:1388-1390.
19. Struhl G, Basler K. Organizing activity of wingless protein in Drosophila. Cell 1993; 72:527-540.
20. Amcheslavsky A, Jiang J, Ip YT. Tissue damage-induced intestinal stem cell division in Drosophila. Cell Stem Cell 2009; 4:49-61.
21. van de Wetering M, Cavallo R, Dooijes D, et al. Armadillo coactivates transcription driven by the product of the Dro-sophila segment polarity gene dTCF. Cell 1997; 88:789-799.
22. Guo Z, Driver I, Ohlstein B. Injury-induced BMP signaling negatively regulates Drosophila midgut homeostasis. J Cell Biol 2013; 201:945-961.
23. Li H, Qi Y, Jasper H. Dpp signaling determines regional stem cell identity in the regenerating adult Drosophila gastrointestinal tract. Cell Rep 2013; 4:10-18.
24. Barker N, Huch M, Kujala P, et al. Lgr5(+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell 2010; 6:25-36.
25. Strand M, Micchelli CA. Regional control of Drosophila gut stem cell proliferation: EGF establishes GSSC proliferative set point & controls emergence from quiescence. PLoS One 2013; 8:e80608.
26. Ren F, Wang B, Yue T, Yun EY, Ip YT, Jiang J. Hippo signaling regulates Drosophila intestine stem cell proliferation through multiple pathways. Proc Natl Acad Sci USA 2010; 107:21064-21069.
27. Karpowicz P, Perez J, Perrimon N. The Hippo tumor suppressor pathway regulates intestinal stem cell regeneration. Development 2010; 137:4135-4145.
28. Buchon N, Broderick NA, Chakrabarti S, Lemaitre B. Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev 2009; 23:2333-2344.
29. Jiang H, Edgar BA. EGFR signaling regulates the proliferation of Drosophila adult midgut progenitors. Development 2009; 136:483-493.
30. Zhou F, Rasmussen A, Lee S, Agaisse H. The UPD3 cytokine couples environmental challenge and intestinal stem cell division through modulation of JAK/STAT signaling in the stem cell microenvironment. Dev Biol 2013; 373:383-393.
31. Dubreuil RR, Grushko T, Baumann O. Differential effects of a labial mutation on the development, structure, and function of stomach acid-secreting cells in Drosophila melanogaster larvae and adults. Cell Tissue Res 2001; 306:167-178.
32. Hoppler S, Bienz M. Specifcation of a single cell type by a Drosophila homeotic gene. Cell 1994; 76:689-702.
33. Bienz M. Endoderm induction in Drosophila: the nuclear targets of the inducing signals. Curr Opin Genet Dev 1997; 7:683-688.
34. Tanaka R, Takase Y, Kanachi M, Enomoto-Katayama R, Shirai T, Nakagoshi H. Notch-, Wingless-, and Dpp-mediated signaling pathways are required for functional specifcation of Drosophila midgut cells. Dev Biol 2007; 304:53-61.
35. Filshie BK, Poulson DF, Waterhouse DF. Ultrastructure of the copper-accumulating region of the Drosophila larval midgut. Tissue Cell 1971; 3:77-102.
36. Shanbhag S, Tripathi S. Epithelial ultrastructure and cellular mechanisms of acid and base transport in the Drosophila midgut. J Exp Biol 2009; 212:1731-1744.
37. Canfield V, West AB, Goldenring JR, Levenson R. Genetic ablation of parietal cells in transgenic mice: a new model for analyzing cell lineage relationships in the gastric mucosa. Proc Natl Acad Sci USA 1996; 93:2431-2435.
38. Bredemeyer AJ, Geahlen JH, Weis VG, et al. The gastric epithelial progenitor cell niche and differentiation of the zymogenic (chief) cell lineage. Dev Biol 2009; 325:211-224.
39. Bardin AJ, Perdigoto CN, Southall TD, Brand AH, Schweis-guth F. Transcriptional control of stem cell maintenance in the Drosophila intestine. Development 2010; 137:705-714.
40. Nyeng P, Norgaard GA, Kobberup S, Jensen J. FGF10 signaling controls stomach morphogenesis. Dev Biol 2007; 303:295-310.
41. Sander GR, Powell BC. Expression of notch receptors and ligands in the adult gut. J Histochem Cytochem 2004; 52:509-516.
42. Kim TH, Shivdasani RA. Notch signaling in stomach epithelial stem cell homeostasis. J Exp Med 2011; 208:677-688.
43. Matsuda Y, Wakamatsu Y, Kohyama J, Okano H, Fukuda K, Yasugi S. Notch signaling functions as a binary switch for the determination of glandular and luminal fates of endodermal epithelium during chicken stomach development. Development 2005; 132:2783-2793.
44. Hongyo T, Buzard GS, Palli D, et al. Mutations of the Kras and p53 genes in gastric adenocarcinomas from a high-incidence region around Florence, Italy. Cancer Res 1995; 55:2665-2672.
45. Lee JW, Soung YH, Seo SH, et al. Somatic mutations of ERBB2 kinase domain in gastric, colorectal, and breast carcinomas. Clin Cancer Res 2006; 12:57-61.
46. Lee WC, Beebe K, Sudmeier L, Micchelli CA. Adenomatous polyposis coli regulates Drosophila intestinal stem cell proliferation. Development 2009; 136:2255-2264.
47. Lin G, Xu N, Xi R. Paracrine Wingless signalling controls self-renewal of Drosophila intestinal stem cells. Nature 2008; 455:1119-1123.
48. Singh SR, Zeng X, Zheng Z, Hou SX. The adult Drosophila gastric and stomach organs are maintained by a multipotent stem cell pool at the foregut/midgut junction in the cardia (proventriculus). Cell Cycle 2011; 10:1109-1120.
49. Takashima S, Mkrtchyan M, Younossi-Hartenstein A, Merriam JR, Hartenstein V. The behaviour of Drosophila adult hindgut stem cells is controlled by Wnt and Hh signalling. Nature 2008; 454:651-655.
50. Zeng X, Chauhan C, Hou SX. Characterization of midgut stem cell-and enteroblast-specifc Gal4 lines in Drosophila. Genesis 2010; 48:607-611.
51. Furriols M, Bray S. A model Notch response element detects suppressor of hairless-dependent molecular switch. Curr Biol 2001; 11:60-64.
52. Yarnitzky T, Min L, Volk T. An interplay between two EGF-receptor ligands, Vein and Spitz, is required for the formation of a subset of muscle precursors in Drosophila. Mech Dev 1998; 79:73-82.
53. Spradling AC, Stern D, Beaton A, et al. The Berkeley Dro-sophila Genome Project gene disruption project: single P-element insertions mutating 25% of vital Drosophila genes. Genetics 1999; 153:135-177.
54. Lee T, Luo L. Mosaic analysis with a repressible neurotechnique cell marker for studies of gene function in neuronal morphogenesis. Neuron 1999; 22:451-461.
55. Lin G, Xu N, Xi R. Paracrine unpaired signaling through the JAK/STAT pathway controls self-renewal and lineage differentiation of Drosophila intestinal stem cells. J Mol Cell Biol 2010; 2:37-49.
56. Wang C, Zhao R, Huang P, et al. APC loss-induced intestinal tumorigenesis in Drosophila: Roles of Ras in Wnt signaling activation and tumor progression. Dev Biol 2013; 378:122-140.